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Abundance and co-occurrence of extracellular capsules increase environmental breadth: Implications for the emergence of pathogens

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Rendueles, Olaya, Garcia-Garcerà, Marc, Néron, Bertrand, Touchon, Marie, Rocha, Eduardo P. C.·2017·PLOS Pathogens
DOI 10.1371/journal.ppat.1006525PMC PMC5542703
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Abstract

Extracellular capsules constitute the outermost layer of many bacteria, are major virulence factors, and affect antimicrobial therapies. They have been used as epidemiological markers and recently became vaccination targets. Despite the efforts to biochemically serotype capsules in a few model pathogens, little is known of their taxonomic and environmental distribution. We developed, validated, and made available a computational tool, CapsuleFinder, to identify capsules in genomes. The analysis of over 2500 prokaryotic genomes, accessible in a database, revealed that ca. 50% of them-including Archaea-encode a capsule. The Wzx/Wzy-dependent capsular group was by far the most abundant. Surprisingly, a fifth of the genomes encode more than one capsule system-often from different groups-and their non-random co-occurrence suggests the existence of negative and positive epistatic interactions. To understand the role of multiple capsules, we queried more than 6700 metagenomes for the presence of species encoding capsules and showed that their distribution varied between environmental categories and, within the human microbiome, between body locations. Species encoding capsules, and especially those encoding multiple capsules, had larger environmental breadths than the other species. Accordingly, capsules were more frequent in environmental bacteria than in pathogens and, within the latter, they were more frequent among facultative pathogens. Nevertheless, capsules were frequent in clinical samples, and were usually associated with fast-growing bacteria with high infectious doses. Our results suggest that capsules increase the environmental range of bacteria and make them more resilient to environmental perturbations. Capsules might allow opportunistic pathogens to profit from empty ecological niches or environmental perturbations, such as those resulting from antibiotic therapy, to colonize the host. Capsule-associated virulence might thus be a by-product of environmental adaptation. Understanding the role of capsules in natural environments might enlighten their function in pathogenesis.

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  • Correlational results from observational data do not prove causation, but correlations can be used within comparative analyses to test causal hypotheses and examine evidence for causality.

    “A general point here is that correlational results from observational data do not prove causation, but correlations can be used within comparative analyses to test causal hypotheses and examine evidence for causality42,90.”

    From A phylogenetic approach to comparative genomics (2025) · cites this paper as [90]

    The Results section on capsule co-occurrence and the Methods section on phylogenetic controls show the authors using comparative associations to test hypotheses. The Discussion says their results are “not consistent with the idea that capsules evolved to facilitate pathogenesis.” The paper thus supports using correlations to assess a causal hypothesis, but the passages do not state the broader methodological point that observational correlations cannot prove causation. (LLM, conf=0.78)

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Cited by

Sorted by citations

Authors
Rendueles, O., Garcia-Garcerà, M., Néron, B., Touchon, M., & Rocha, E. P. C.
Affiliations
  • Centre National de la Recherche Scientifique (FR)
  • Institut Pasteur (FR)
Corresponding author
Rendueles, Olaya
ORCID
Venue
PLOS Pathogens
Publisher
Public Library of Science (PLoS)
Published
2017-07-24
Volume
13
Issue
7
Pages
e1006525
ISSN
  • 1553-7366 (ISSN-L)
  • 1553-7374
DOI
10.1371/journal.ppat.1006525
PMC
PMC5542703
OpenAlex
W2739330082
Cited by
89
References
0
Citations by year
2026: 15 · 2025: 12 · 2024: 15 · 2023: 7 · 2022: 7 · 2021: 10 · 2020: 12 · 2019: 5 · 2018: 6
FWCI
4.69
Type
journal article
Language
en
Update notices
new_version (2017-08-03)
Open access
Licence
Locations
  • PLoS Pathogens (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
  • European Research Council (281605)
  • Fondation pour la Recherche Médicale (ARF20150934077)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Immunology and Microbiology › Microbiology › Microbial infections and disease research
Keywords
bacterial capsule, prokaryotic genomes, epistasis, metagenome, human microbiome, opportunistic pathogens, virulence factors, environmental adaptation, antibiotic therapy, pathogen emergence
MeSH terms
Bacteria, Bacterial Infections, Bacterial Proteins, Humans, Phylogeny, Virulence, Bacterial Capsules, Genome, Bacterial

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